Path integration and lesions within the head direction cell circuit: Comparison between the roles of the anterodorsal thalamus and dorsal tegmental nucleus.

Abstract

Experiments were designed to determine whether 2 regions of the head direction cell circuit, the anterodorsal thalamic nucleus (ADN) and the dorsal tegmental nucleus (DTN), contribute to navigation. Rats were trained to perform a food-carrying task with and without blindfolds prior to receiving sham lesions or bilateral lesions of the ADN or DTN. ADN-lesioned rats were mildly impaired in both versions of the task. DTN-lesioned rats, however, were severely impaired and showed reduced heading accuracy in both task versions. These findings suggest that although both the DTN and ADN contribute to navigation based on path integration and landmarks, disruption of the head direction cell circuit at the level of the DTN has a significantly greater effect on spatial behavior than lesions of the ADN.

Selective disconnection of the hippocampal formation projections to the mammillary bodies produces only mild deficits on spatial memory tasks: Implications for fornix function

“…The dorsal nucleus of Gudden is thought to be necessary for generating the head-direction signal (e.g., Bassett et al, 2007) and, hence, is required for tasks that require path integration (Frohardt et al, 2006). Despite the consensus that head-direction information is integral for effective navigation and the potential use of directional information to solve some of the present spatial tasks (Hamilton et al, 2008), lesions of the lateral mammillary body, which block head-direction information (e.g., Blair et al, 1998), have only mild effects on the tasks used in the present study (Vann, 2005).…”

Lesions of the Tegmentomammillary Circuit in the Head Direction System Disrupt the Head Direction Signal in the Anterior Thalamus

“…1), which is thought to intermingle with the mlf as it enters the DTN ventrally (Cruce, 1977). Frohardt et al (2006) described two cases in which the mlf was deliberately interrupted without damaging the DTN and found the animals to be unimpaired on a DTN-dependent spatial task, suggesting functional independence of the DTN and mlf. The adjacent ventral tegmental nucleus of Gudden exhibits a parallel projection pattern to the medial mammillary nucleus, which in turn projects to the anteroventral thalamus.…”

The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation

“…However, a major limitation to interpreting these studies as demonstrating that HD cells are used in navigation comes from the absence of specificity afforded by a lesion. For example, lesions to areas such as the mammillary bodies [21] or anterior thalamus [18,20] likely have broader effects on learning and memory in addition to their effects on HD cells [37,38]. In addition, if the effects that these lesions have on behavior are due to knocking out the HD signal, it is unclear why lesions further upstream in the network have greater effects than lesions in, for example, downstream cortical regions [20].…”

“…The other approach to explore the role of HD cells in behavior has shown that lesions of areas involved in the HD signal leads to various deficits in spatial ability [18][19][20][21]. However, a major limitation to interpreting these studies as demonstrating that HD cells are used in navigation comes from the absence of specificity afforded by a lesion.…”

“…Correlations between place cell firing and spatial behavior, especially in relation to goaldriven behavior [16], have prompted recent work showing that there is a causal link between place cells and an animal's sense of location [17]. However, despite numerous lesion studies showing indirect evidence that the HD circuit might be involved broadly in spatial processing [18][19][20][21], a direct causal role of the HD signal as a neural compass that guides directional behavior has not been demonstrated yet.…”